International l o u m a l of Osteoarchaeology Vol2: 2 3 - 3 0 (19921

Microscopical Findings Associated with the Diagnosis of Osteoporosis in Pa I aeo pat hol og y CHARLOTTE ROBERTS' and JENNIFER WAKELY' 'Calvin Wells Laboratory, Department of Archaeological Sciences, University of Bradford, Bradford 8 0 7 lDP, UK; and 'Department of Anatomy & School of Archaeological Studies, University of Leicester, University Road, Leicester L E l 9HN, UK

ABSTRACT This paper presents some preliminary results on microscopical identification of microfractures in human skeletal remains which may be associated with osteoporosis. A technique is described for the examination of cancellous bone and applied to a number of vertebrae and one radius. All the material used is Romano-British or English medieval. However, microscopical screening for osteoporosis could form a useful part of comparative studies on historically or geographically different populations. The archaeological significance of osteoporosis in terms of skeletal ageing and nutritional status is discussed.

Keywords: Osteoporosis, Palaeopathology, Microfractures, Diagnosis

Introduction

Osteoporosis is a loss of bone mass occurring when resorption of bone exceeds deposition in the process of skeletal remodelling and turn- over. Bone growth and maintenance are sensi- tive to a wide range of physiological and en- vironmental factors, some of which can cause osteoporosis.

Commonly, it is associated with ageing, developing in women after the fifth decade and in both sexes after the age of seventy. In females its onset is associated with reduced oestrogenic hormone output after the menopause. It is a common cause of ill-health in the elderly in modern populations.'-6

It might be expected that osteoporosis would be less common in pre-historic and early historic populations where fewer individuals apparently lived beyond middle age than in contemporary developed countries. However, osteoporosis in the young can be a skeletal indicator of mal- nutrition, whether a general lack of protein and calories or a more specific deficiency of calcium

or Vitamin D needed for osteogenesis. In such conditions it particularly affects young women because of the demands of pregnancy and lac- tati~n.~.' ' A number of studies already docu- ment the occurrence of osteoporosis, shown by changes in the microstructure or mineral con- tent of bones from the archaeological record, particularly in American material,11-16 using its occurrence in the young as an indicator of nutritional stress, in both sexes.

Morphologically, osteoporosis presents as an increase in the size and number of spaces in compact bone and as trabecular loss in cancel- lous (spongy) bone. In the latter, load-bearing trabeculae are affected later than those which do not support body weight. There is an increased risk of fracture, particularly of the distal radius, femoral neck and vertebral bodies, giving the usual modern clinical presentation of a patient suffering from osteo- porosis. Affected vertebrae may collapse and repair in a compressed form (Figure I).

Microfractures of trabecular bone occur when bone is subjected to stress, and can be more

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1047-482X/92/010023-08$05.00 @ 1992 by John Wiley & Sons, Ltd

Received 10 November 1990 Accepted 22 September 1991

24 C. Roberts and I. Wakely

Figure 1. The interior of an osteoporotic lumbar vertebra (Baldock, 1136) showing fine, widely spaced trabeculae. The section also shows the superiorhnferior flattening characteristic of vertebral collapse.

common when the bone is weakened by osteo- porosis. Microscopical examination of a series of modern osteoporotic vertebrae’’ showed micro- fractures of individual trabeculae, healing by means of nodular aggregates of spongy bone around the fracture site. Observations by light microscopy (LM) and scanning electron micro- scopy (SEM), to be described in this paper, show a morphologically identical phenomenon in lum- bar vertebral bodies from burials from Raunds, Northamptonshire (Medieval), Kingsholm, Gloucester (Romano-British), Baldock, Hert- fordshire (Romano-British) and Ashton, Northamptonshire (Romano-British), not all of which showed the external compression that would identify them as osteoporotic to the naked eye. A radius showing a Colles’ fracture from the Kingsholm Cemetery was similarly affected. These observations both add to our knowledge of the health of the particular

individuals involved, and indicate the value of the microscopical study of spongy bone in larger scale studies of osteoporosis in human skeletal remains.

Criteria for age and sex

The sex of individuals was determined by exam- ination of the morphology of the skull and pelvis; when available, metrical data, particularly of the femur, were used in problematical cases.

The age of individuals was assessed using currently available methods. These consisted of the later fusing epiphyses and dental develop- ment, molar tooth attrition, degeneration of the pubic symphysis and sternal ends of the ribs and the presence of degenerative joint disease (all summarized in Ref. 21). All these methods have limitations in their use but it was considered

Osteoporosis 25

appropriate to use this multimethod approach. The use of each method was obviously depen- dent on the completeness of the skeleton. It is recognized that ageing of adult skeletons is problematical and, therefore, assigning a speci- fic age or age range to an individual was not considered appropriate. For the purposes of this paper, ‘older adult’ may be assumed to be an individual who was over 50 years of age at death.

Techniques of examination

Whilst thin sectioning’’ is the method of choice for assessment of the structure of compact bone, a technique using thick slices is preferable for cancellous bone because of the greater volume of material available for examination in any one specimen.

Slices, 0.5-1.0 cm thick, were cut by hand from the bones with a hacksaw and cleaned and

prepared for SEM a s in a previous study of normal vertebral

Before coating with gold for SEM, the slices were examined under a binocular dissecting microscope for signs of osteoporosis. Areas of trabecular thinning or nodular swellings on individual trabeculae were mapped on an out- line drawing of the slice, which was used for localization and orientation in the scanning electron microscope.

Images at magnifications from 8x to 300x were recorded on Kodak Technical Pan film in an IS1 DS 130 scanning electron microscope operated at 15 kV.

Results

Raunds Burial No. 52 7 7 : Older adult - female Two slices were obtained from the first lum- bar vertebral body. Whilst not externally

Figure 2. A trabecula from the radius of Kingsholm skeleton 251, showing area of osteoclastic resorption (arrowed).

26 C. Roberts and 1. Wukely

Figure 3. A microfracture callus from the third lumbar vertebra of Raunds skeleton 5085. The arrow shows a collar of woven bone around a thickened trabecula.

compressed, it showed internal evidence of osteoporosis in the structure of the spongiosa. Throughout the bone the trabeculae were fine and sparse, especially in the centre. Vertical trabeculae were thicker and more numerous than horizontal trabeculae. Some interrupted trabeculae were observed; of these, some with broken ends were clearly artefacts of sectioning. O n the other hand, those with rounded or pointed ends covered with an intact bone surface were products of ante-mortem bone remodelling. In this specimen, as in others examined in this study, areas of osteoclastic resorption (Howship’s lacunae) were frequently seen (Figure 2).

Three healing microfractures on vertical trabeculae were seen. Two were nodular aggregates of woven bone around the trabecula and the third was a slight fusiform thickening

with a surface similar to that of trabecular bone elsewhere in the specimen.

Raunds Burial No. 5085: Older adult - male The vertebra (L3) showed no external flattening or other signs of osteoporosis and, internally, the majority of trabeculae were broad and plate- like, as expected in a male skeleton.23 In the middle third of the vertebra, extending back as far as the posterior venous channel, there was a localized area of fine, widely separated trabeculae within which two healing micro- fractures were seen. Both consisted of a well- developed collar of woven bone around the trabecula (Figure 3).

Ashton Burial No. 205: Mature adult - male

Two vertebrae, T6 and L1, were available from

Osteopovosis 27

Figure 4. A well-healed bead-like microfracture callus on a trabecula from the first lumbar vetebra of Ashton skeleton 205 (arrowed). Several interrupted trabeculae are also present.

this skeleton. Whilst the thoracic vertebra showed a normal profile, the body of the lumbar vertebra was anteriorly wedged, suggesting some degree of osteoporosis. Internally, the trabeculae were extremely sparse with many empty areas, especially in the centre. One well- healed microfracture was seen among many thin and interrupted trabeculae in the middle third of the section. It appeared as a smooth bead-like thickening (Figure 4).

Kingsholm Burial No. 251 : Older adult - female

Two lumbar vertebrae, L 1 and L4, and the right radius were examined. The radius showed a healed Colles’ fracture (Figure 5 ) . The vertebral bodies were compressed, especially L4.

In the radius, the distal end was filled with trabecular bone. A band of dense bone marked

the site of the united fracture. Two trabeculae, aligned with the long axis of the bone, showed broad thickenings identified as healed micro- fractures.

The first lumbar vertebra showed no micro- fractures and little trabecular thinning. The fourth was extremely osteoporotic, with most of the spongiosa consisting of thin and widely spaced trabeculae. Four separate microfracture calluses were recorded from this specimen, intermediate in form between the woven bone seen in Figure 3 and a smooth bead as in Figure 4.

Discussion

Normal vertebral ageing, exaggerated in senile osteoporosis, involves the loss of centrally- situated trabeculae from the vertebral body

28 C. Roberts and I. Wakely

Figure 5. The Colles' fracture in skeleton 251 from Kingsholm. Gloucester

before those around the periphery, and the horizontal before the vertical trabeculae. This sequence has been observed in modern mater- ia12,17'18 and archaeological s ~ e c i m e n s . ~ ~ ' ~ ~ In this way, weight-bearing structures are conserved and vertebral collapse does not necessarily occur, even in severe osteoporosis. Only 5-10 per cent of the 60 per cent of elderly women showing wedge-shaped vertebrae as a result of osteo- porosis will develop actual crush A recent osteoarchaeological example of a crush fracture2' is actually in a male skeleton.

The presence of healing microfractures on vertical trabeculae indicates a repair mechanism for preserving the structural soundness of those mechanically important structures. We believe that the differing morphologies that we have observed represent stages in the healing pro- cess, enabling the study of dynamic changes in the skeleton at the cellular level.

Standard ageing methods, relying in all the cases studied on pubic symphysis morphology, dental wear or other biological indications of age, have placed three of the skeletons in the '45+' category at death, suggesting a possible association with senility and postmenopausal changes in the females.

The method illustrated in this study shows the potential of the microscopical study of skeletons in screening skeletal populations for osteoDorosis. thus enabling its studv in associa-

tion with age, nutrition or other forms of biological stress. The method is also useful in the study of the palaeoepidemiology of frac- tures.

The question of the specificity of the associa- tion of microfractures with osteoporosis must be addressed. They can occur in healthy, young bone as a result of high levels of mechanical stress on the cancellous bone. As always, the palaeopathological findings must be looked at in the context of the whole skeleton. Skeleton Raunds 5085 is an interesting example here because of the presence of microscopical changes in the vertebra of an aged individual without other evidence of osteoporosis. It is possible that the changes are simply the result of minor trauma induced by stress, but osteo- porosis at a level undetectable by clinical meth- ods cannot be discounted.

Diagnosis is less of a problem with the present method than it is with radiography because we are examining the structure of the bone, not simply assessing mineral density as in a radio- graph. We suggest that the presence of micro- fracture calluses in vertebrae with no external signs of osteoporosis, along with thinned trabeculae within an otherwise normal-for-age structure, may be a way of detecting early changes before overall mineral density is reduced or external form changed by structural collause. Uu to 30 Der cent of bone mass has to be

25

Ost eo po rus is 2 9

lost before a radiograph reveals bone change. In addition, the problem of distinguishing ante- mortem bone change from postmortem damage can make radiography an unreliable diagnostic method for palaeopathology.

While the use of whole vertebrae is inevitably destructive, one advantage of our method is that i t can be used on already fragmented bones, if their origin is identifiable, without losing fur- ther valuable specimens.

Acknowledgements The authors wish to thank Mr G. L. C. McTurk for operation of the IS1 DS 130 microscope in the University of Leicester Scanning Electron Microscope Unit; Jean Brown, photographer in the Department of Archaeological Sciences, University of Bradford, for reproducing the photographs for this paper; Ann Stirland for permission to examine the Ashton specimen and the Gloucester City Excavation Unit and the Northamptonshire Archaeology Unit for the Kingsholm and Raunds specimens. It is also a pleasure t o thank Miss M. Reeve for typing the manuscript and M r N. Cockcroft for technical assistance in the Department of Anatomy, University of Leicester.

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